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Hyperparasitism Behaviour of the Autoparasitoid Encarsia Tricolor on Two Secondary Host Species

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Hyperparasitism Behaviour of the Autoparasitoid Encarsia Tricolor on Two Secondary Host Species View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Wageningen University & Research Publications BioControl DOI 10.1007/s10526-008-9189-2 Hyperparasitism behaviour of the autoparasitoid Encarsia tricolor on two secondary host species Ying Huang Æ Antoon J. M. Loomans Æ Joop C. van Lenteren Æ Xu RuMei Received: 19 November 2006 / Accepted: 23 July 2008 Ó International Organization for Biological Control (IOBC) 2008 Abstract Hyperparasitism by virgin female Encar- However, rates of hyperparastism were different sia tricolor was studied by direct observation of its according to host stage and host species. Hosts in behaviour when contacting two secondary host the late larval stages were most preferred for species (Encarsia formosa and E. tricolor) at diffe- hyperparasitization and the heterospecific E. formosa rent host stages (first and second larval stage, third was more preferred as a secondary host than the larval stage, and pupal stage). The searching and conspecific, E. tricolor, in particular from the prepu- hyperparasitism behavioural sequence of E. tricolor pal stage onwards. The window of vulnerability, i.e., was independent of the host stage of the whitefly the duration of the period in which a secondary host (Aleyrodes proletella), and was similar to several is susceptible to hyperparasitism, was largely deter- related primary parasitoid species. In experiments mined by the occurrence and rate of melanization with equal numbers of secondary hosts, encounter after the onset of pupation. The duration of a frequencies were equal for both secondary host successful hyperparasitization event was longer than species in all developmental stages observed. one that failed. Superparasitism occurred only once in all cases. The potential effect of autoparasitoids on biological control programs and the consequences for Handling editor: Torsten Meiners. selection and release of an effective, yet ecologically safe agent are discussed. Y. Huang Institute of Animal and Plant Quarantine, Chinese Academy of Inspection and Quarantine, Beijing, Peoples Keywords Encarsia formosa Á Hymenoptera Á Republic of China Aphelinidae Á Autoparasitoid Á Hyperparasitoid Á Behaviour Á Aleyrodes proletella Á Y. Huang Á A. J. M. Loomans (&) Á J. C. van Lenteren Laboratory of Entomology, Wageningen University, Environmental effects Wageningen, The Netherlands e-mail: [email protected] Y. Huang Á X. RuMei College of Life Science, Beijing Normal University, Introduction Beijing, Peoples Republic of China It is commonly believed that the application of Present Address: biological control is a safe alternative to pesticides, A. J. M. Loomans Department of Entomology, Plant Protection Service, and a wide range of parasitoids has been released Wageningen, The Netherlands successfully as biological control agents (Gurr and 123 Y. Huang et al. Wratten 2000). Several species of aphelinid parasi- parasitoids (hyperparasitoids) on larvae or pupae of toids have been used to help suppress populations their own or other primary parasitoid species. Mated of the two most economically important whitefly female autoparasitoids may lay both fertilized and species, Trialeurodes vaporariorum (Westwood) unfertilized eggs, but virgin females can only lay (greenhouse whitefly) and Bemisia tabaci (Gennadius) unfertilized eggs in secondary hosts (Gerling 1966). (tobacco whitefly) (both Hemiptera: Aleyrodidae; It is generally thought that parasitoids with hyper- e.g. Gerling et al. 2001; van Lenteren and Woets parasitic behaviour are injurious in biological control 1988; van Lenteren et al. 1996). A number of these programs (Luck et al. 1981) and it is standard parasitoids are members of the genus Encarsia quarantine procedure to exclude exotic obligate (Fo¨rster), such as Encarsia formosa (Gahan) hyperparasitoids from biological control programmes (Hymenoptera: Aphelinidae). Whereas the economic (Sullivan and Vo¨lkl 1999). However, several auto- benefits are clear, the ecological effects of an introduced parasitoid species have been successfully introduced species on the indigenous fauna are not. During the past as biological control agents (Bogra´n and Heinz decades, Howarth (1991) and others argued that the 2002), some introductions have, however, resulted import and release of exotic species for biological in problems, such as those of Encarsia pergandiella control might create problems for the indigenous fauna. Howard. The latter species was imported into Italy to Recent reviews show that such exotic natural enemies control the greenhouse whitefly, but established have in some cases causednegative effects on non-target outside, and can now be found all around the organisms and the environments (Louda et al. 2003; Mediterranean Area (Portugal, Spain, Italy, France, van Lenteren et al. 2006). Tunesia) (Loomans and van Lenteren 1999), With regard to biological control of exotic green- regionally upsetting successful biological control house whiteflies in Europe, the introduced species applications by primary parasitoids in greenhouses E. formosa may encounter native species of whiteflies (Gabarra et al. 1999, 2003). In New Zealand there as well as native parasitoids, like Encarsia tricolor have been several instances where E. pergandiella (Fo¨rster). The possibility of such interactions raises has been present in significant numbers on green- several questions: Will the exotic and indigenous house tomato crops and although large introductions parasitoids coexist, or will one of them lose the of E. formosa were made weekly, control of the pest competition and will it be displaced? What will the was lost (John Thompson, personal communication effect be on the dynamics of indigenous whitefly 2005). populations? And what kind of effect has the exotic The host range of autoparasitoids is much wider biological control agent on the indigenous ecosystem? and multitrophic effects are larger than that of These questions are related to the interactions between primary parasitoids, because of their heteronomous species of parasitoids at the level of parasitoid hyperparasitoid behaviour. Therefore, the concern behaviour, life history and the interaction between about the direct and indirect ecological effects of these parasitoids and their hosts (Murdoch 1996). autoparasitoids in biological control remains wide Another question we are faced with is what the open (Rosen 1981). Since autoparasitoids occupy two effect could be of the release of an exotic primary trophic levels, it is not proper to separate the overall parasitoid on the population dynamics and survival of interactions into several two-species interactions facultative autoparasitoids. This question relates to (host-parasitoid or primary-hyperparasitoid) (Hassell the rather typical biology of several aphelinid para- 2000). We propose to study such relationships from sitoids (e.g. Hunter and Kelly 1998). Males and two viewpoints: (1) the effect of two competing females of hymenopteran parasitoid species in the parasitoids for one primary host; (2) and the effects of Aphelinidae develop in or on different kinds of hosts, the interactions between a primary and a hyper- and are therefore called heteronomous hyperparasi- parasitoid (secondary parasitoid) (Fig. 1; May and toids, more specifically autoparasitoids (Hunter and Hassell 1981). Woolley 2001). Fertilized female eggs develop as In the current study we considered the relationship obligate primary parasitoids on their primary hosts, between an exotic biological control agent (the whiteflies or scale insects. On the other hand, strictly primary parasitoid E. formosa) and a native unfertilized male eggs develop as secondary parasitoid (the facultative autoparasitoid E. tricolor) 123 Hyperparasitism behaviour comparison of the behavioural strategy towards conspecific and heterospecific secondary hosts may facultative be used also to clarify the issues on the role of autoparasitoid autoparasitoids in biological control mentioned above. From both systems mentioned (Avilla and Copland 1987; Williams 1991)—directly or, as in the unmated Avilla’s paper, indirectly—a preference emerged of E. tricolor females towards heterospecific secondary hosts for male egg oviposition. Behavioural observa- tions will assist in testing the hypothesis that primary parasitoid autoparasitoids can discriminate between species of (secondary host) secondary hosts to reduce self-hyperparasitism and henceforth this preference may negatively affect the outcome of a biological control programme. We specifically studied the host preference of the native autoparasitoid E. tricolor when offered different secondary host species, and the effect that different life stages of the host may have on this preference. primary host Materials and methods Fig. 1 Diagram to illustrate the relationships of a three- Insect and plant rearing species system, which is containing an autoparasitoid (after May and Hassell 1981) The cabbage whitefly, Aleyrodes proletella, was used as primary host. It was cultured on cabbage (Brussels on a native host (the cabbage whitefly, Aleyrodes sprouts, Brassica oleracea gemmifera cv. Cyrus) in a proletella L.). The autoparasitoid E. tricolor is widely greenhouse at 21°C and 16L:8D. As primary parasi- distributed throughout the West Palaearctic region. toids we used E. formosa and E. tricolor females. Females are solitary endoparasitoids of several E. formosa was obtained from a commercial company whitefly species, including A. proletella, Aleurotuba (EnStripÒ, Koppert
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